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Low Testosterone Associated With Obesity and the Metabolic Syndrome Contributes to Sexual Dysfunction and Cardiovascular Disease Risk in Men With Type 2 Diabetes

  1. Christina Wang, MD1⇓,
  2. Graham Jackson, MD2,
  3. T. Hugh Jones, MD3,
  4. Alvin M. Matsumoto, MD4,
  5. Ajay Nehra, MD5,
  6. Michael A. Perelman, PHD6,
  7. Ronald S. Swerdloff, MD1,
  8. Abdul Traish, PHD7,
  9. Michael Zitzmann, MD8 and
  10. Glenn Cunningham, MD9
  1. 1Division of Endocrinology, Department of Medicine, Harbor-UCLA Medical Center and Los Angeles Biomedical Research Institute, Torrance, California
  2. 2London Bridge Hospital, London, U.K.
  3. 3Robert Hague Centre for Diabetes and Endocrinology, Barnsley Hospital, and the Department of Metabolism, University of Sheffield Medical School, Sheffield, U.K.
  4. 4Geriatric Research, Education and Clinical Center, V.A. Puget Sound Health Care System, Department of Medicine, University of Washington School of Medicine, Seattle, Washington
  5. 5Department of Urology, Mayo Clinic, Rochester, Minnesota
  6. 6Departments of Psychiatry, Reproductive Medicine, and Urology, NY Weill Cornell College of Medicine, New York, New York
  7. 7Department of Urology, Boston University School of Medicine, Boston, Massachusetts
  8. 8Clinical Andrology/Centre for Reproductive Medicine and Andrology, University Clinics of Muenster, Muenster, Germany
  9. 9Departments of Medicine and Molecular and Cellular Biology, Baylor College of Medicine, St. Luke’s–Baylor Diabetes Program, Houston, Texas
  1. Corresponding author: Christina Wang, wang{at}labiomed.org.
Diabetes Care 2011 Jul; 34(7): 1669-1675. https://doi.org/10.2337/dc10-2339
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    Figure 1

    Complex multidirectional interactions between testosterone and obesity, metabolic syndrome, and type 2 diabetes mediated by cytokines and adipokines leading to comorbidities such as ED and increased CVD risk. FFA, free fatty acids; GnRH, gonadotropin-releasing hormone; LH, luteinizing hormone; PAI-1, plasminogen activator inhibitor-1.

Tables

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  • Table 1

    Low testosterone is associated with increased mortality in older men

    Study designnFollow-up (years)MortalityHazard ratio (95% CI)Recent studies
    Retrospective8588All-cause1.88 (1.34–2.63)*Shores et al. (42)
    Prospective79420All-cause and CVD1.40 (1.14–1.71)*
1.38 (1.02–1.85)*Laughlin et al. (45)
    Prospective2,31410All-cause and CVD2.29 (1.60–3.26)*Khaw et al. (43)
    Prospective1,9547.2All-cause and CVD2.32 (1.38–3.89)*Haring et al. (44)
    Prospective9306.9All-cause and CVD in men with CVD2.27 (1.45–3.60)*Malkin et al. (46)
    • ↵*On the basis of recent publications in which the number of subject is >500 and age of the subjects is >60 years.

  • Table 2

    Randomized trials of testosterone replacement in hypogonadal men with metabolic syndrome or type 2 diabetes

    StudyKapoor et al. (55)Heufelder et al. (56)Kalinchenko et al. (57)Jones et al.* (37)
    SubjectsType 2 diabetesNew type 2 diabetes/metabolic syndromeType 2 diabetes/metabolic syndromeType 2 diabetes/metabolic syndrome
    Study designRCT-cNRCTRCT-pRCT-p
    n2432184220
    Duration (months)31266/12*
    Medications for diabetesDiet, oral, insulinNaiveDiet, oralDiet, oral
    Baseline serum testosterone (nmol/L)≤8.6≤10.5≤6.7≤10.2
    Testosterone formulationTES injections (200 mg/2 weeks)Testosterone gel (50 mg/day)TU depot injectionsTestosterone gel (40–80 mg/day)
    Treatment effects (changes)
     HOMA-IR−1.7−0.9−1.49−0.54
     Fasting glucose (nmol/L)−1.6−0.3 (AS)↔−0.42 (AS)
     Fasting insulin (mIU/mL)↔↓↔↓(AS)
     HbA1c−0.37−0.80ND↔ [−0.45]†
     Total cholesterol (nmol/L)−0.4ND↔↔ [−0.13]
     LDL cholesterol (nmol/L)↔ND↔↔‡
     HDL cholesterol (nmol/L)↔↑§↔−0.049‡
     Triglycerides↔↓↔↔
     Lipoprotein aNDNDND↓
     BMI↔↔↔↔
     Waist circumference↓↓↓↔
     % Body fatNDNDND↔
     Blood pressure↔↓‖ND↔
    • ↔, No significant change; ↑, significant increase; ↓, significant decrease; AS, approaching significance (P = 0.05–0.07); ND, not done; NRCT, randomized open label, not placebo-controlled parallel trial; RCT-c, randomized placebo-controlled crossover; RCT-p, randomized placebo-controlled parallel; TES, mixed testosterone esters; TU, testosterone undecanoate depot injections after the first injection followed by another injection at 6 weeks and then injections every 12 weeks. Testosterone gel was dose-adjusted to give total testosterone level >17 nmol/L.

    • ↵*The study by Jones et al. (TIMES2) had no medication changes in the first 6 months unless overriding clinical needs, but medication changes were allowed in the second 6 months for ethical reasons (intention-to-treat group, modified per protocol group where no changes in medications occurred; data not shown).

    • ↵†Significant difference compared with placebo observed after 9 months, but result may be confounded by allowed medication changes.

    • ↵‡Metabolic syndrome subgroup showed significant changes in total cholesterol (−0.34 mmol/L), LDL cholesterol (−0.21 mmol/L), and HDL cholesterol (−0.058 mmol/L).

    • ↵§No figure quoted.

    • ‖Diastolic blood pressure only.

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Low Testosterone Associated With Obesity and the Metabolic Syndrome Contributes to Sexual Dysfunction and Cardiovascular Disease Risk in Men With Type 2 Diabetes
Christina Wang, Graham Jackson, T. Hugh Jones, Alvin M. Matsumoto, Ajay Nehra, Michael A. Perelman, Ronald S. Swerdloff, Abdul Traish, Michael Zitzmann, Glenn Cunningham
Diabetes Care Jul 2011, 34 (7) 1669-1675; DOI: 10.2337/dc10-2339

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Low Testosterone Associated With Obesity and the Metabolic Syndrome Contributes to Sexual Dysfunction and Cardiovascular Disease Risk in Men With Type 2 Diabetes
Christina Wang, Graham Jackson, T. Hugh Jones, Alvin M. Matsumoto, Ajay Nehra, Michael A. Perelman, Ronald S. Swerdloff, Abdul Traish, Michael Zitzmann, Glenn Cunningham
Diabetes Care Jul 2011, 34 (7) 1669-1675; DOI: 10.2337/dc10-2339
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